A behavioural study to help clarify how undersowing with clover affects host-plant selection by pest insects of brassica crops

Laboratory and field-cage tests were done to determine how undersowing brassica plants (Brassica oleraceae L. and B. rapa L.) (Cruciferae) with subterranean clover (Trifolium subterraneum L.) (Papilionaceae) affected host-plant selection by eight pest insect species of brassica crops. The pest species tested were Pieris rapae (Lepidoptera: Pieridae) (the small white butterfly), Pieris brassicae (Lepidoptera: Pieridae) (the large white butterfly), Delia radicum (Diptera: Anthomyiidae) (the cabbage root fly), Phaedon cochleariae (Coleoptera: Chrysomelidae) (the mustard beetle), Plutella xylostella (Lepidoptera: Yponomeutidae) (the diamond-back moth), Evergestis forficalis (Lepidoptera: Pyralidae) (the garden-pebble moth), Mamestra brassicae (Lepidoptera: Noctuidae) (the cabbage moth) and Brevicoryne brassicae (Hemiptera: Aphididae) (the cabbage aphid). In all tests, except two in which the brassica plants were about three times as high as the clover background, 39%–100% fewer of the pest insect stage monitored were found on host plants presented in clover than on those presented in bare soil. Contrary to claims supporting the ‘enemies hypothesis’, differences in colonization alone appeared sufficient to account for the lower numbers of insects found when host plants are undersown with clover. To be effective in reducing plant colonization, the clover must cover 50%, and preferably more, of the vertical profile of the crop plants. As clover used as an undersown crop often has to be cut to make it less competitive with the main brassica crop, temporal aspects of the condition of the clover during critical periods of pest activity need to be recorded carefully before concluding that undersowing does not produce the effect desired against certain pest species under field conditions. The effective clover barrier is like any other treatment, if it is not present at the appropriate time it cannot be expected to reduce pest insect numbers.     

A cabbage root fly oviposition deterrent in the frass of garden pebble moth caterpillars

The cabbage root fly, Delia radicum (L.), was deterred from laying eggs on cauliflower plants sprayed with a water-soluble extract of the frass of caterpillars of the garden pebble moth, Evergestis forficalis (L.), which had fed on a range of cruciferous species. Chemical analysis of the extract revealed the presence of a phenolic acid which was not present in the frass of larvae of two other Lepidoptera (Mamestra brassicae (L.) and Plutella xylostella (L.)) that had fed on the same range of cruciferous plants. The deterrent chemical was isolated and identified as sinapic (3,5-dimethoxy-4-hydroxycinnamic) acid. Spraying cauliflower plants with a buffered solution of the acid in water (0.1, 1 and 10 mM) reduced the numbers of cabbage root fly eggs laid by 60–70%. In field experiments, the deterrent effect persisted 5 days after leaves were sprayed with a buffered, aqueous solution of the acid (10 mM).

---

Résumé D. radicum L. a pondu beaucoup moins sur des choux-fleurs pulvérisés avec un extrait (polaire) hydrosoluble d'excréments de chenilles de E. forficalis L. qui avaient consommé différentes crucifères. La pulvérisation des choux-fleurs avec une suspension aqueuse d'éluate de méthanol d'une colonne polyamide et d'éluate aqueux d'une colonne florosile a réduit respectivement de 50 et 66% le nombre d'oeufs pondus. L'analyse chimique des fractions actives révèle la présence d'un acide phénolique isolé et identifié comme acide sinapique (3,5-diméthoxy-4-hydroxycinnamique). Cet acide est absent des excréments des chenilles de Mamestra brassicae L. et Plutella xylostella L. qui avaient consommé la même gamme de crucifères. La pulvérisation des plants de choux-fleurs par une solution aqueuse tamponnée d'acide sinapique a réduit la ponte de D. radicum de 60 à 70%. Dans la nature, l'effet dissuasif persiste sur choux-fleurs 5 jours après la pulvérisation avec une solution aqueuse tamponnée à 10 mM d'acide sinapique.

     

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

Effects of nitrogen and foliar biomass on population parameters of cabbage insects

The effects of different nitrogen (N) fertilization rates (0, 45, 90, and 168 kg N/ha), plant nitrogen concentration, and plant biomass on abundance and population growth of diamondback moth, Plutella xylostella (L.), cabbage looper, Trichoplusia ni (Hübner), cabbage budworm, Hellula phidilealis (Walker), imported cabbageworm, Artogeia rapae (L.), and cross-striped cabbageworm, Evergestis rimosalis (Guenée), were investigated in Homestead and Sanford, Florida in 1987. The effects of these factors on the parasitization of P. xylostella were also examined. In Homestead, abundance of most insect pests and parasitized P. xylostella increased with an increase in the level of N applied and with an increase in plant biomass. Similar results were found in Sanford, although results were not consistently significant. Abundance of most insect pests was significantly positively correlated with plant N concentration. Multiple regression analyses indicated that foliar biomass was significantly more important than N fertilization rate and subsequent plant N concentration at predicting abundance of insect pests and parasitized P. xylostella on cabbage.     

Effects of intercropping white cabbage with clovers on pest infestation and yield

During two consecutive years the effects of intercropping fresh market white cabbage with two species of clover on pest populations and yield were studied. White cabbage cv. Minicole was intercropped withTrifolium repens (white clover) andTrifolium subterraneum (subterranean clover) as compared to the monocrop. During the season observations were made on pest population developments, especially ofMamestra brassicae L. (cabbage moth),Brevicoryne brassicae L. (cabbage aphid),Delia brassicae L. (cabbage root fly), and evaluation of caterpillar feeding injury. At harvest the yield in quantity and quality was determined to be able to assess the gross financial result. Intercropping effects in terms of suppression of oviposition and larval populations of various pests were found. Although no pesticides were used and competition reduced the weight, the quality of the intercropped cabbages lead to a better financial result compared to the monocropped cabbage crop. The results are discussed in the perspective of the practical implications in the context of IPM.     

Effect of belowground herbivory on parasitoid associative learning of plant odours

Root herbivores can influence both the performance and the behaviour of parasitoids of aboveground insect herbivores through changes in aboveground plant quality and in the composition of the plant's odour blend. Here we show that root herbivory by Delia radicum larvae did not influence the innate preferences for plant odours of the two closely related parasitoid species Cotesia glomerata and C. rubecula, but did affect their learned preferences, and did so in an opposite direction. While C. glomerata learned to prefer the odour of plants with intact roots, C. rubecula learned to prefer the odour of root‐infested plants. The learned preference of C. glomerata for the odour of plants with intact roots matches our previously published result of its better performance when developing in P. brassicae hosts feeding on this plant type. In contrast, the relatively stronger learned preference of C. rubecula for the odour of root‐infested plants cannot be merely explained by its performance, as the results of our present study indicate that D. radicum root herbivory did not influence the performance of C. rubecula nor of its host P. rapae. Our results stress the importance of assessing the influence of root herbivores on both innate and learned responses of parasitoids to plant odours.     

Plant traits shape soil legacy effects on individual plant–insect interactions

Plant-mediated soil legacy effects can be important determinants of the performance of plants and their aboveground insect herbivores, but, soil legacy effects on plant–insect interactions have been tested for only a limited number of host plant species and soils. Here, we tested the performance of a polyphagous aboveground herbivore, caterpillars of the cabbage moth Mamestra brassicae, on twelve host plant species that were grown on a set of soils conditioned by each of these twelve species. We tested how growth rate (fast- or slow-growing) and functional type (grass or forb) of the plant species that conditioned the soil and of the responding host plant species growing in those soils affect the response of insect herbivores to conditioned soils. Our results show that plants and insect herbivores had lower biomass in soils that were conditioned by fast-growing forbs than in soils conditioned by slow-growing forbs. In soils conditioned by grasses, growth rate of the conditioning plant had the opposite effect, i.e. plants and herbivores had higher biomass in soils conditioned by fast-growing grasses, than in soils conditioned by slow-growing grasses. We show that the response of aboveground insects to soil legacy effects is strongly positively correlated with the response of the host plant species, indicating that plant vigour may explain these relationships. We provide evidence that soil communities can play an important role in shaping plant–insect interactions aboveground. Our results further emphasize the important and interactive role of the conditioning and the response plant in mediating soil–plant–insect interactions.     

Determining the host‐plant resistance mechanisms for Mamestra brassicae (Lepidoptera: Noctuidae) pest in cabbage

Six cabbage (Brassica oleracea var. capitata) varieties with different levels of resistance to Mamestra brassicae (Lepidoptera: Noctuidae) were investigated in order to assess whether antibiosis and antixenosis mechanisms are involved in the resistance to this pest or not. Four experiments were conducted to determine the effect of variety and plant ontogeny on larval behaviour, adult oviposition and leaf damages in non‐choice and choice tests. Larval survival, time to development and larval weights differed depending on the varieties and plant stages that we tested. At the pre‐head stage, larval mortality was higher, larvae died faster, time to pupation was shorter, pupae were lighter and the percentage of viable pupae and growth index (GI) values were lower than larvae reared from plants at the head stage. The commercial hybrid ‘Corazón de buey’ and the local variety named ‘BRS0535’ exhibited antibiosis to M. brassicae as they reduced its survival and growth and delayed its development time. In addition, these varieties were the most resistant after artificial infestation in terms of head foliage consumption and number of larvae per plant. Oviposition tests demonstrated that resistance found in ‘Corazón de buey’ and BRS0535 could be also based on antixenosis mechanisms as they resulted in fewer egg batches on plants, whereas BRS0402 could be classified as resistant because M. brassicae larvae showed less preference for it. Thus, resistance to M. brassicae found in cabbage crops may be due to the joint action of several factors involving antibiosis and antixenosis. We found significant differences in the resistance of BRS0535 depending on the plant ontogeny as it loses its resistance while developing. Further studies are required to identify the mechanism of antibiotic resistance which is present in this variety at the pre‐head stage and the changes that occur in plant defence as it grows.     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.

     

Response of Brassica oleracea to temporal variation in attack by two herbivores affects preference and performance of a third herbivore

1. Plants are frequently under attack by multiple insect herbivores, which may interact indirectly through herbivore‐induced changes in the plant's phenotype. The identity, order, and timing of herbivore arrivals may influence the outcome of interactions between two herbivores. How these aspects affect, in turn, subsequently arriving herbivores that feed on double herbivore‐induced plants has not been widely investigated. 2. This study tested whether the order and timing of arrival of two inducing herbivores from different feeding guilds affected the preference and performance of a subsequently arriving third herbivore, caterpillars of Mamestra brassicae L. (Lepidoptera: Noctuidae). Aphids [Brevicoryne brassicae L. (Hemiptera: Aphididae)] and caterpillars [Plutella xylostella L. (Lepidoptera: Yponomeutidae)] were introduced onto wild Brassica oleracea L. (Brassicaceae) plants in different sequences and with different arrival times. The effects of these plant treatments on M. brassicae caterpillars were assessed in pairwise preference tests and no‐choice performance tests. 3. The caterpillars of M. brassicae preferred to feed from undamaged plants rather than double herbivore‐induced plants. Compared with undamaged plants, they preferred plant material on which aphids had arrived first followed by caterpillars, whereas they avoided plant material with the reverse order of herbivore arrival. Performance of the caterpillars increased with increasing arrival time between herbivore infestations in double herbivore‐induced plants. Although M. brassicae grew faster on plants induced by aphids than on those induced by caterpillars alone, its performance was not affected by the order of previous herbivore arrival. 4. These results imply that the timing of colonisation by multiple herbivores determines the outcome of plant‐mediated herbivore–herbivore interactions.     

Engineering of benzylglucosinolate in tobacco provides proof-of-concept for dead-end trap crops genetically modified to attract Plutella xylostella (diamondback moth)

Glucosinolates are biologically active natural products characteristic of crucifers, including oilseed rape, cabbage vegetables and the model plant Arabidopsis thaliana. Crucifer‐specialist insect herbivores, like the economically important pest Plutella xylostella (diamondback moth), frequently use glucosinolates as oviposition stimuli. This suggests that the transfer of a glucosinolate biosynthetic pathway to a non‐crucifer would stimulate oviposition on an otherwise non‐attractive plant. Here, we demonstrate that stable genetic transfer of the six‐step benzylglucosinolate pathway from A. thaliana to Nicotiana tabacum (tobacco) results in the production of benzylglucosinolate without causing morphological alterations. Benzylglucosinolate‐producing tobacco plants were more attractive for oviposition by female P. xylostella moths than wild‐type tobacco plants. As newly hatched P. xylostella larvae were unable to survive on tobacco, these results represent a proof‐of‐concept strategy for rendering non‐host plants attractive for oviposition by specialist herbivores with the long‐term goal of generating efficient dead‐end trap crops for agriculturally important pests.     

Scale-dependent responses in cabbage herbivores affect attack rates in spatially heterogeneous systems

Herbivorous insects face a dilemma when selecting suitable hosts in a complex environment, and their sensory capability may often reduce the female capacity for proper selection. As a consequence, eggs are often deposited on inferior hosts, affecting both insect and host plant fitness. We examined the attack rates of three cabbage herbivores in monocultures and biculture plots of different Brassica oleracea genotypes, with different spatial heterogeneity. The main goals of the study were to improve our understanding of the spatial scales involved in herbivore search processes and to examine the possibility of using spatial heterogeneity for manipulating pest attack rates in cabbage cropping systems. The results showed that the host selection behaviour of the small white butterfly (Pieris rapae) was strongly dependent on spatial heterogeneity. The difference in egg density between plant genotypes was larger when contrasting plants were growing in close proximity than in monoculture. This suggests that P. rapae is able to differentiate among genotypes from a small distance, while selection is compromised at larger spatial scales. The two other herbivores in the study (Mamestra brassicae and Delia radicum) did not respond to heterogeneity at any spatial scale, but showed a constant preference hierarchy. This suggests that host selection in these species occurs after direct plant contact. The difference in species’ responses to spatial heterogeneity has consequences both for selection gradients in natural communities and for the potential to reduce pest attack in polyculture systems.     

The Genome of the Lepidopteran Mamestra brassicae has a Vertebrate-like Content of Methyl-cytosine

Mamestra brassicae genomic DNAs, isolated from larvae and adult tissues and from in vitro cultured CRL-8003 cells, were enzymatically hydrolysed to nucleosides that were separated by HPLC. HPLC analysis showed that 5mC content in cabbage moth larvae, adults and cultured cells was 8.9±0.5, 9.3%±0.2 and 10.2%±0.4 respectively. Cabbage moth 5mC content results the highest reported till now in insects and it is similar to the typical vertebrate one. Analysis of MspI and HpaII restriction pattern on M. brassicae DNA showed that a portion of its genome was methylated at CpG sites. Moreover, the absence of small digestion products after MspI digestion suggested that CpG are not clustered in the cabbage moth genome. Finally, methylation of repeated DNAs has been studied. Comparison of the restriction pattern of MspI and HpaII after hybridisation with the hobo, mariner, 28S and 5S rDNA probes did not evidence any difference indicating the absence of CpG methylation in all the studied repeated DNAs.     

Heterorhabditid Behavior in the Presence of the Cabbage Maggot,Delia radicum, and its Host Plants

The behavior of Heterorhabditis zealandica Poinar strain T327 was investigated in the presence of the cabbage maggot, Delia radicum L., and plants that are susceptible to D. radicum infestation. Newly formed puparia and freeze-killed third instar larvae were attractive to infective nematodes. Newly harvested infective nematodes did not respond to the puparia, whereas 1-month-old and 2-month-old nematodes reached the insect targets within 15 minutes. There were no significant differences in the ability of similar-sized, third instar larval D. radicum and Galleria mellonella L., the greater wax moth, to attract nematodes. There was a tendency for a greater number of insects to attract more nematodes. The roots of ball cabbage and radish were equally attractive to nematodes, but rutabaga roots neither attracted nor repelled the nematodes. Germinated seeds of radish attracted nematodes, and there was a tendency for more numerous germinated seeds to attract more nematodes.     

Trap cropping to control Delia radicum populations in cruciferous crops: first results and future applications

This study evaluates the efficacy of a new approach to the control of Delia radicum populations. We suggest associating the primary crop with a trap crop that is expected to be more attractive to D. radicum females and to attract and sustain their natural enemies such as Aleochara bilineata and A. bipustulata. Various cruciferous species were compared in terms of their preference for adult D. radicum females, and performance, as estimated by larval survival. Laboratory results were complemented by field experiments in which the selected trap crops were associated with broccoli plants. The following results were obtained. Of the six different cruciferous plant species tested, Delia radicum females showed a strong preference for Chinese cabbage, with turnip also being attractive. Following the laboratory results, turnip was chosen as a trap crop because it was easier to cultivate and presented good preference and performance. In the field experiments, Aleochara adults were present in higher numbers in plots associated with turnips than in pure broccoli plots. The presence of Aleochara adults in plots with turnips improved plant protection; as fewer broccoli plants were attacked, the attacked plants were less severely damaged, and more D. radicum pupae were parasitised than in pure broccoli plots. Delia radicum females did not lay fewer eggs on broccoli plants associated with turnips. Moreover, protection and parasitism were more effective in the rows closest to the central row of turnips, suggesting that Aleochara adults limit their activity to its immediate vicinity.     

Aboveground herbivory affects indirect defences of brassicaceous plants against the root feeder Delia radicum Linnaeus: laboratory and field evidence

1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far. 2. Lab and field studies were conducted to examine whether the presence of the leaf herbivore Pieris brassicae Linnaeus on brassicaceous plants influences the response of Trybliographa rapae Westwood, a specialist parasitoid of the root feeder Delia radicum Linnaeus. 3. The present results show that the attraction of the parasitoid towards host‐infested plants disappeared when these plants were also infested by P. brassicae. This absence of attraction was observed both when the complete odour blend or only undamaged leaves from damaged plants were offered, emphasising the role of systemically induced volatiles for host location in T. rapae. 4. Furthermore, the field study revealed that parasitism levels dropped from 30% on root‐infested plants to 4% on double‐infested plants. 5. The present study is the first to confirm that reduced attraction to host‐infested plants as a result of simultaneous attack by below‐ and aboveground herbivores translates into lower levels of parasitism in the field.     

Contrary effects of jasmonate treatment of two closely related plant species on attraction of and oviposition by a specialist herbivore

Elevated jasmonic acid (JA) concentrations in response to herbivory can induce wounded plants to produce defences against herbivores. In laboratory and field experiments we compared the effects of exogenous JA treatment to two closely related cabbage species on the host‐searching and oviposition preference of the diamondback moth (DBM), Plutella xylostella. JA‐treated Chinese cabbage (Brassica campestris) was less attractive than untreated Chinese cabbage to ovipositing DBM, while JA‐treatment of common cabbage (B. oleracea) made plants more attractive than untreated controls for oviposition by this insect. Similar effects were observed when plants of the two species were damaged by DBM larvae. In the absence of insect‐feeding, or JA application, Chinese cabbage is much more attractive to DBM than common cabbage. Inducible resistance therefore appears to occur in a more susceptible plant and induced susceptibility appears to occur in a more resistant plant, suggesting a possible balance mechanism between constitutive and inducible defences to a specialist herbivore.     

Effects of organic and conventional fertilizer treatments on host selection by the aphid parasitoid Diaeretiella rapae

The type and quantity of fertilizer supplied to a crop will differ between organic and conventional farming practices. Altering the type of fertilizer a plant is provided with can influence a plant’s foliar nitrogen levels, as well as the composition and concentration of defence compounds, such as glucosinolates. Many natural enemies of insect herbivores can respond to headspace volatiles emitted by the herbivores’ host plant in response to herbivory. We propose that manipulating fertilizer type may also influence the headspace volatile profiles of plants, and as a result, the tritrophic interactions that occur between plants, their insect pests and those pests’ natural enemies. Here, we investigate a tritrophic system consisting of cabbage plants, Brassica oleracea, a parasitoid, Diaeretiella rapae, and one of its hosts, the specialist cabbage aphid Brevicoryne brassicae. Brassica oleracea plants were provided with either no additional fertilization or one of three types of fertilizer: Nitram (ammonium nitrate), John Innes base or organic chicken manure. We investigated whether these changes would alter the rate of parasitism of aphids on those plants and whether any differences in parasitism could be explained by differences in attractivity of the plants to D. rapae or attack rate of aphids by D. rapae. In free‐choice experiments, there were significant differences in the percentage of B. brassicae parasitized by D. rapae between B. oleracea plants grown in different fertilizer treatments. In a series of dual‐choice Y‐tube olfactometry experiments, D. rapae females discriminated between B. brassicae‐infested and undamaged plants, but parasitoids did not discriminate between similarly infested plants grown in different fertilizer treatments. Correspondingly, in attack rate experiments, there were no differences in the rate that D. rapae attacked B. brassicae on B. oleracea plants grown in different fertilizer treatments. These findings are of direct relevance to sustainable and conventional farming practices.